(Circulation. 1995;91:171-175.)
© 1995 American Heart Association, Inc.
Articles |
Relation of Ultrasonic Backscatter and Acoustic Propagation Properties to Myofibrillar Length and Myocardial Thickness
From the Medical College of Wisconsin (P.D.O'B., D.C.W., K.B.S.), Milwaukee, Wis; the University of Illinois (W.D.O'B.Jr.) (Urbana); and General Electric, Inc (T.L.R.), Milwaukee, Wis.
Correspondence to Kiran B. Sagar, MD, Medical College of Wisconsin, Division of Cardiology, 8700 W Wisconsin Ave, Box 123, Milwaukee, WI 53226.
 |
Abstract |
|---|
 Top Abstract IntroductionMethods Results Discussion References |
|---|
Background Ultrasonic backscatter demonstrates a cardiac cycle–dependent modulation. The exact mechanism of the modulation is under debate. The objective of the present study was to test the hypothesis that a change in size and configuration of myofilaments from systole to diastole alters acoustic propagation properties and backscatter.
Methods and Results In vivo measurements were made of integrated backscatter at 5 MHz (IBR5), followed by in vitro measurements of ultrasonic attenuation, speed, and heterogeneity index using a scanning laser acoustic microscope at 100 MHz. Studies were performed in canine hearts (16) arrested in systole (8) with calcium chloride or arrested in diastole (8) with potassium chloride. Sarcomere length was measured with a calibrated eyepiece on a Ziess microscope. Wall thickness was measured with calipers. The attenuation coefficient of 220±34 dB/cm during systole was significantly higher than the coefficient of 189±24 dB/cm during diastole (P<.01); the IBR5 of -44.7±1.2 dB during systole was significantly greater than the IBR5 of -47.0±1.0 dB during diastole (P<.01); the ultrasonic speed of 1591±11 m/s during systole was higher than the speed of 1575±4.2 m/s during diastole (P<.01); and the heterogeneity index of 7.4±1.8 m/s during systole was significantly lower than the index of 9.0±2.0 m/s during diastole (P<.02). The sarcomere length of 1.804±0.142 µm during diastole was significantly higher than the length of 1.075±0.177 µm during systole (P<.01). Wall thickness was significantly greater during systole than during diastole (20±3 versus 9±3 mm, P<.01).
Conclusions Ultrasonic backscatter and propagation properties are directly related to sarcomere length and myocardial thickness and may be responsible for cardiac cycle–dependent variation in backscatter.
Key Words: backscatter • ultrasound • tissue propagation • myofilaments
|
Introduction |
|---|
|
TopAbstractIntroductionMethods Results Discussion References |
|---|
Ultrasonic backscatter demonstrates a modulation across the cardiac cycle,1 and this modulation closely follows changes in myocardial contractility.2 This modulation in backscatter is abolished during myocardial ischemia.1 2 The exact mechanism of modulation in ultrasonic backscatter with cardiac cycle is under debate. Wickline and associates3 argue that the change in acoustic impedance, which in turn is related to changes in passive elastance with contraction, is responsible for the modulation of ultrasonic backscatter. In studies of isolated papillary muscle, Wear and coworkers4 have shown that modulation occurs in isotonically contracting muscles and not in isometrically contracting muscle. In vitro studies by O'Donnell and others5 provide frequency dependence data that support Shung and Reid's suggestion6 that backscatter arises from small cylindrical scatters. Based on the shape of the backscatter frequency-response and time-varying statistics, the in vivo work from our laboratory argues for a geometric model in which multiple small structures, such as myofilaments, are responsible for myocardial backscatter.7 The present study was designed to test the hypothesis that cyclic variation in backscatter is dependent on active contraction, ie, changes in size and configuration of myofilaments from systole to diastole alter acoustic propagation properties and backscatter. The acoustic propagation properties of myocardium during systole and diastole were measured with a scanning laser acoustic microscope (SLAM), which operates at a frequency of 100 MHz. The SLAM provides acoustic and optical images plus attenuation coefficient, speed of sound, and heterogeneity index data. Conventional imaging frequencies of 3 to 7 MHz were studied using a well-described integrated backscatter measurement (IBR5, or integrated backscatter Rayleigh spectral intensity measurement, referred to 5 MHz).
|
Methods |
|---|
|
TopAbstractIntroductionMethods Results Discussion References |
|---|
Experimental Protocol
Adult mongrel dogs of either sex weighing 15 to 25 kg were anesthetized with phenobarbital sodium (30 mg/kg IV) supplemented with 5 mg/kg per hour IV and ventilated with Harvard Apparatus respirator model 607. Atelectasis was prevented by maintaining an end-respiratory pressure of 5 to 7 cm H2O. A thoracotomy was performed in the left fifth intercostal space, and the lungs were gently retracted. The heart was suspended in a pericardial cradle.
IBR5 was measured by
coupling the transducer to the epicardial surface
of the left ventricle from the left anterior descending coronary artery
(LAD) and left circumflex coronary artery (LCx) territories. A research
prototype instrument was used to measure IBR5; the details have been
published,2 8 and a brief description follows. After
in
vivo measurements were made, hearts were arrested during systole (8)
and during diastole (8). Systolic arrest was produced by rapid
intravenous infusion of calcium chloride (20 to 40 µmol/L). Diastolic
arrest was produced by rapid intravenous injection of potassium
chloride. Myocardial wall thickness was measured with calipers.
Approximately square, transmural tissue samples (5x5 mm multiplied by
wall thickness) for electron microscopic and SLAM examination were
obtained from the regions of LAD and LCx, with the surfaces of the
sample oriented along the axis of the ventricle as shown in Fig
1A
and 1B. The SLAM samples were mounted with
their
endocardial surfaces against a circular cork with Ames Tissue-Tek
O.C.T. (optimal cutting temperature; a polyvinyl alcohol, benzalkonium
chloride, and polyethyleneglycol gel—an embedding medium for frozen
tissue specimens). The base and apical sides of the samples were
carefully marked on the corks. The samples were frozen in liquid
nitrogen, placed into Ziploc bags, and shipped on dry ice from the
Medical College of Wisconsin to the Bioacoustics Research Laboratory at
the University of Illinois for storage in a Revco freezer at -70°C
until analysis.
|
Immediately before SLAM analysis, each tissue specimen was removed from the freezer, and the corks were mounted on an object disk of a Lipshaw cryostat (maintained at -35°C). Approximately 50 to 100 µm of the upper surface of the specimen was sectioned and discarded to provide a flat, even surface for subsequent sections. Consequently, all subsequent sections were from planes parallel to the endocardial and epicardial surfaces and of known orientation. This procedure ensured that all specimens remained frozen between the times of initial freezing and the SLAM analysis. Previous studies have shown that rapid freezing in liquid nitrogen has no effect on the ultrasonic impedance and other mechanical properties of several different tissues.9 10 Specimens of known thicknesses (50, 75, 100, 200, and 400 µm) were mounted on a 1-in2 sheet of mylar (25 µm thick) with albumin fixative and marked so that the depth within the wall and the orientation relative to the axis of the ventricle were known.
Sarcomere Length
Tissue specimens
(5x5 mm) were also obtained for measurement of
sarcomere length. Sarcomere length was determined on samples fixed in
glutaraldehyde. Fixed muscle tissue was minced in iso-osmotic glycerol
(0.28 mol/L) and then briefly (
5 seconds) ground with a Polytron
homogenizer. The resulting suspension of fixed myofibril fragments was
allowed to settle for 5 minutes to remove air bubbles, and then a drop
of the suspension was placed on a slide and covered with a coverslip.
Sarcomere length was measured with a calibrated eyepiece micrometer on
a Ziess microscope at a total magnification of 2000x (10x
eyepiece,
2x multiplier, and 100x lens). Sarcomere length was determined on
myofibrils with four to eight clearly defined sarcomeres by measuring
the total length and dividing by the number of sarcomeres included.
Only myofibrils with clearly defined Z-lines, A bands, and I bands were
measured or counted. A minimum of 20 myofibrils with a total of at
least 100 sarcomeres were measured for each sample.
Ultrasonic Backscatter Instrumentation and Data Analysis
In
vivo ultrasonic backscatter was measured using a research
instrument used in previous studies.2 8 The
myocardium was
examined with a 6-mm-diameter, unfocused circular transducer that was
fitted with a water-filled fixture that maintained the transducer
approximately 18 mm from the epicardium. Echoes were range-gated on the
midmyocardium, thus avoiding the specular echoes at the endocardial and
epicardial surfaces. The prototype obtained echo signals with a
0.5-µsec resolution and a uniform bandwidth extending from 4.0 to 6.5
MHz. A digitized ECG waveform was used to synchronize the data
acquisition with the QRS complex. Backscatter echoes were performed at
evenly spaced intervals over 16 cardiac cycles, and data were stored
for later analysis.
According to previous methods,2 8 the echoes were adjusted using calibration data7 and further adjusted for the frequency effects of tissue absorption, diffraction, and power-law scattering, resulting in measurements of absolute reflectivity integrated over the frequency spectrum from 4.0 to 6.5 MHz. This is called the IBR5 and represents an absolute measure of the backscatter in square centimeters of reflecting surface per cubic centimeter of volume.11 The IBR5 was constructed at selected ranges and expressed in decibels.
The magnitude and phase of the cardiac amplitude modulation of the IBR5 measurements were determined by independently averaging the IBR5 signals from six evenly spaced phases of the cardiac cycle (relative to the midpoint of the QRS complex). The Fourier coefficient for the amplitude modulation (of the fundamental of the cardiac cycle) was determined by mean square fit to the six data points. The ratio of the IBR5 at the positive and negative peaks of the Fourier sine wave (expressed in decibels) was used as an index of the amplitude modulation and called the Fourier coefficient of amplitude modulation. Also, the phase of the Fourier coefficient was measured from the negative peak of the Fourier sine wave to the QRS complex and expressed as a percent of the cardiac cycle.
Scanning Laser Acoustic Microscope
A SLAM (Sonomicroscope
100, Sonoscan, Inc), operating at an
ultrasonic frequency of 100 MHz, was used to determine the specimen's
attenuation coefficient, propagation speed, and heterogeneity index.
Operational details of the SLAM have been
published.11 12 13 14 15 16
Briefly, the specimen is placed on a sonically activated fused silica
stage along with a thin layer of normal saline and covered with a
semireflective coverslip. A focused scanning laser beam probe detects a
dynamic ripple (surface displacement) by reflection from the
coverslip's lower surface. The reflected laser beam is processed to
yield the acoustic image, from which the attenuation coefficient is
determined, and the interference image, from which the speed and
heterogeneity index are determined. The laser-transmitted beam also is
transmitted through the specimen to yield an optical image. All three
images are displayed in real time on a standard television monitor
representing a specimen area measuring approximately 3 mm
horizontally by 2 mm vertically (typically 100x). A frame grabber is
used to digitize the video signal of the acoustic and interference
images17 and performs frame averaging (up to 256 frames),
convolutions (for filtering), and histograms (for dynamic range
determination). In addition, attenuation coefficient, speed, and
heterogeneity index estimations are performed with software using the
digitized video image.
Attenuation Coefficient
An
insertion loss procedure is used to estimate the attenuation
coefficient.12 15 Attenuation coefficient is a
measure of
energy loss per unit distance (decibels per meter). In principle, this
procedure compares the received signal amplitude of the specimen of
known thickness in the sound path with that of the reference medium,
normal saline. A subimage area of approximately 400x250 µm (96
pixels horizontally by 32 pixels vertically) in the acoustic image is
used. The signals received from the subimage area are digitized to
yield an average amplitude value (V) expressed in decibels. A minimum
of five V values are recorded for normal saline. The specimen is then
moved into the subimage area, and a minimum of three V values are
recorded at each of five specimen locations. An insertion loss (IL)
value, given in decibels, is estimated from the following:
 |
where Vr is the average V value recorded from normal saline, and Vs represents individual V values from the specimen. This process yields five IL values for each specimen thickness. Five specimen thicknesses ranging from 50 to 400 µm are used, and the slope of IL versus specimen thickness (using a linear least-squares fit with all 25 IL thickness values) yields the attenuation coefficient.
Speed
The spatial
frequency domain technique is used to yield speed
from the interference image.13 15 Speed represents
propagation of ultrasound (in meters per second). The 2x3-mm field of
view contains approximately 39 vertical interference lines equally
spaced by about 85 µm. The propagation speed is estimated by the
horizontal shift of the fringe lines relative to where the fringe lines
would be without the specimen, ie, relative to the reference (with
known speed value) medium. The specimen is positioned so that each
interference line includes both the reference fluid above and below the
specimen. From the digitized interference image, basically each
interference line is digitized and processed, yielding a vertical
(relative to the image orientation) speed profile. For each sample,
five specimen thicknesses are analyzed, with each yielding a mean speed
value from the speed profile region within the specimen. The individual
mean speed values are then averaged to yield the ultrasonic speed of
that sample.
Heterogeneity Index
The heterogeneity
index represents an estimate of the
spatial distribution of the ultrasonic speed.11 An
advantage of determining the ultrasonic speed using the speed profile
is that many speed values, each representative of a 4x8-µm
specimen region, are obtained. Not only is the mean value estimated,
yielding speed, but also the standard deviation is estimated. This
standard deviation of the spatial speed distribution is an estimate of
the heterogeneity index of the specimen at the specified thickness.
The values of the heterogeneity index are an inverse function of thickness. Therefore, the separate heterogeneity index values are reported, at a thickness of 100 µm as representative of all thicknesses.
Uncertainty
Estimates of attenuation
coefficient and speed from the SLAM
have been assessed for solutions of known acoustic properties and
duplicate samples of skin and healing wound tissue.15 With
a homogeneous medium, the accuracy (proximity to the true value) was
±2.9% and the precision (reproducibility of successive independent
measurements) was ±0.4% for speed; for attenuation coefficient,
accuracy and precision were ±12% and ±15%, respectively. With
heterogenous samples of normal canine skin and wound tissue, the speed
and attenuation coefficient precision were ±1.7% and ±16%,
respectively.
Statistical Analysis
All SLAM values and sarcomere length
values are reported as
mean±SD. Comparison between systolic and diastolic measurements were
performed with a paired t test, and changes were considered
significant when values were P<.05.
|
Results |
|---|
|
TopAbstractIntroductionMethods Results Discussion References |
|---|
Ultrasonic attenuation coefficient, speed, heterogeneity index, IBR5, sarcomere length, and wall thickness were measured in 16 dogs. A total of 32 data sets were obtained for each parameter—16 during systole and 16 during diastole.
Fig 2A shows the attenuation coefficient and IBR5 during
systole and during diastole. Attenuation coefficient of 220±34 dB/cm
during systole was significantly higher than the coefficient of 189±24
dB/cm during diastole (P<.01). IBR5 of -47±1.0 dB
during
systole was significantly weaker than the IBR5 of -44.7±1.2 dB
(P<.01) during diastole.
|
Ultrasonic speed of 1591±11 m/s during systole was about 1% higher
than the speed of 1575±4.2 m/s during diastole; the difference is
small but statistically significant (P<.01) (Fig
2B
). The
heterogeneity index of 7.4±1.8 m/s during systole was significantly
lower than the index of 9.0±2.0 m/s during diastole
(P<.02) at a specimen thickness of 100 µm (Fig
2B). This
gradient in heterogeneity index between systole and diastole was
observed for all specimen thicknesses.
Sarcomere length and wall thickness are shown in Fig 3.
As expected, the sarcomere length of 1.804±0.142 µm during diastole
was significantly higher than the length of 1.075±0.177 µm during
systole, thus confirming the change in sarcomere size with contraction.
Wall thickness was significantly greater during systole than during
diastole (20±3 versus 9±3 mm, P<.01; Fig
3).
|
Regional variability in acoustic propagation properties was determined by comparing specimens from territories supplied by LAD and LCx. No significant regional differences were observed for any of the parameters.
|
Discussion |
|---|
|
TopAbstractIntroductionMethods Results Discussion References |
|---|
The above data show that cardiac cycle–dependent changes in myofilament length and thickness are associated with modulation in acoustic propagation properties and ultrasonic backscatter. Attenuation coefficient and ultrasonic speed are higher in systole, whereas heterogeneity index and IBR5 are lower in systole.
Myocardial contraction causes several alterations in the cardiac muscle: increased thickness and tissue density, changes in collagen matrix, change in size, and shape of ultrasonic scatterer within the myofilament. Any of these changes alone or in combination can alter attenuation, speed, heterogeneity index, and backscatter. This report suggests a geometrical model for the cardiac cycle dependence of backscatter seen at frequencies of 3 to 7 MHz.
A compilation of the attenuation coefficient, speed, and protein and water concentrations in various tissues indicates that the attenuation coefficient and speed in tissue increase as the protein concentration increases and water decreases.18 19 Collagen also plays an important role in the acoustic properties of tissues. The higher the collagen content, the higher are the attenuation, speed, and backscatter. During systole, the muscle is expected to be most dense. In systole, myocardium has higher density, the collagen and protein per unit mass of the muscle are higher, and thus attenuation coefficient is greater. The attenuation measured by SLAM is roughly 15% higher (in terms of decibels) in systole. Mass density also plays a role in the speed of propagation. At the SLAM frequency of 100 MHz, the alteration of the ultrasonic speed is on the order of 1%, with the higher speed occurring in systole. Because speed is reciprocal to the square root of the product of mass density and compressibility, the product of density and compressibility must be about 2% higher in systole than in diastole. It appears that in systole there is an increase in mass density and a decrease in compressibility. Systolic decrease in compressibility may arise from alteration in collagen cross-linkage or non-Hookien behavior of the elastic elements as contraction distorts the elastic components of the myocardium.3
It is possible that cyclic variation in backscatter could be related to myocardial tissue attenuation and possible cyclic changes in attenuation.3 20 In the present study, attenuation was significantly greater in systole, although it was not as high as predicted by Wickline and associates.3 However, when one calculates the cyclic backscatter that arises from the measured attenuation, it is insufficient to account for the cyclic backscatter observed at frequencies of 3 to 7 MHz, as suggested by Wickline et al.3 Consequently, variation in attenuation alone is not sufficient basis for cyclic backscatter. Thus, it does not appear that either the attenuation or propagation speed properties directly address the mechanisms of cyclic backscatter.
Wickline and associates3 suggested that cyclic variation in backscatter was related to myofibrillar elastic characteristics. They speculated that cyclic backscatter changes arise from an impedance mismatch between intracellular and extracellular domains, with the intracellular domain associated with the series elastic components and the extracellular domain associated with parallel elastic components, of a Maxwell-type model for the myocardium. The change in acoustic impedance of elastic components due to differential stretching and compression should give rise to the observed cyclic variation. However, Wear and associates4 reported little cyclic variation in backscatter for isometrically contracting canine muscle, where the series elastic components should have been cyclically stretched while parallel components were held fixed. By the model of Wickline et al, this should have produced a cyclic variation in the intracellular and extracellular acoustic impedance. We suspect that the basis of cyclic backscatter may not be due to this mechanism.
Mottley and Miller21 delineated an angular dependence
relative to the muscle fiber orientation. The present study
demonstrates a change in size and thickness of myofilaments with
contraction but does not directly address the question of anisotropy of
the scatterers. The samples were sectioned in planes parallel to the
endocardial surface (see Fig 1), which ensured that muscle
fiber
orientation was always in the plane of the sections. The in vivo data
were similarly obtained with the ultrasound traversing the myocardial
wall at a normal incidence. Thus, the sound waves in both IBR5 and SLAM
analyses were always perpendicular to the fibers, removing this
variable from the investigation.
The SLAM operates at 100 MHz and produces images with an acoustic resolution of approximately 29 µm. The paired acoustic and optical images were evaluated to determine if the backscatter, which is seen in clinical cardiac images at frequencies from 2.5 to 7.5 MHz, could be ascribed to structures resolved by the SLAM at 100 MHz. It has been reported by our laboratory that the through transmission acoustic images of the myocardium were of very low contrast, which delineated fiber margins and general structure, and correlated well with these features in the paired optical images.11 Consequently, it is concluded that the basis of myocardial backscatter is not resolvable at the 29-µm level and that the backscatter must arise from structures that are much smaller. In addition, previous work at our laboratory shows that the backscatter exhibits almost Rayleigh scattering, indicating that the scattering elements are much smaller than a wavelength (one-fourth wavelength at 5 MHz is 77 µm).7 This study suggests that the basis of ultrasonic backscatter may be at the myofibrillar level.
Heterogeneity index and ultrasonic backscatter are weaker during systole than during diastole. The heterogeneity index is a through transmission marker for backscatter, with the variation in transmission indicating that energy is being removed from the through transmitted ultrasound by the backscatter. The relatively higher index during diastole indicates more backscatter than during systole, which is consistent with the cyclic modulation of myocardial backscatter in IBR5 data. Consequently, the SLAM data support the conclusion that the basis of the backscatter is at the ultrastructural level. Moreover, SLAM acoustic images previously reported by these researchers11 clearly indicate lineal structures following the muscle fibers of the paired optical image. The small size of scatterers is consistent with previously reported data5 7 concerning the spectral shape of the backscattering spectra, as discussed above. Moreover, the scattering spectra obtained independently in systole and diastole maintain the same shape, with the diastolic spectrum being stronger everywhere than the systolic spectrum.7 This indicates that in cyclic backscatter, the elemental scatterers alter the product of their scattering size and density.
The basis of backscatter is the impedance mismatch at the surface of a scattering element. The surface area of each small scattering element determines its reflectivity to the ultrasound. The total backscatter is the summation of the reflection intensities of all the elements in a given volume (thus, IBR5 has the dimensions of area per volume). Data from our laboratory7 indicate that it is the product of scatterer area and scatterer density that is altered by the contraction. It is proposed that a "geometric" model be used to account for cyclic backscatter, based primarily on changes in the density of scatterers with contraction.
Available knowledge indicates that clinical backscatter arises from
small scatterers that are linearly arranged, which most likely are the
collagenous connective tissues plus other heavy molecules, such as the
mycin and actin fibers of the active contracting elements. Each of
these small scattering objects presents a given scattering surface
area to the ultrasound, and the summation of the intensity of
individual reflections makes up the overall backscatter. The scattering
elements are present in the microstructure with other nonreflecting
material, such as mitochondria (40% of myocardium), intracellular
and extracellular fluids, and so on. Systolic contraction results in
the partial compression and partial reshaping of the noncontracting
constituents of the ultrastructure, and this contributes to the gross
thickening of the myocardial wall. Consequently, in the contracted
state, there is greater mean free distance separating connective
tissues and myofilaments. Increased separation constitutes a reduction
in the number of reflecting elements in a given volume, which is the
scatterer density. One index of this density is wall thickening with
contraction, which, in the present study, was a thickening of a
factor of 2. It would be expected that the density of scatterers
would be reduced approximately by this factor of 2. The observed change
in the intensity of IBR5 is a factor of 1.7 (ie, 2.3 dB), which is
consistent with the change of scatterer density. The lack of cyclic
variation in backscatter with isometric contraction is also consistent
with this hypothesis.
In future studies, it may be possible to accurately correlate cyclic changes in tissue histology with the proposed geometric model of cyclic backscatter. In particular, variation in the mean free spacing of suspected scattering components with contraction is of interest, as well as myofibril dimensional and density changes.
|
Acknowledgments |
|---|
This work was supported in part by National Institutes of Health grant HL-39014. We thank Kathi Annous and Sandra Wilton for technical assistance and Cindy Ketola for preparing the manuscript.
Received May 12, 1994; accepted July 27, 1994.
|
References |
|---|
|
TopAbstractIntroductionMethods Results Discussion References |
|---|
1. Barzilai B, Madaras EI, Sobel BE, Miller JG, Perez JE. Effects of myocardial contraction on ultrasonic backscatter before and after ischemia. Am J Physiol. 1984;247:H478-H483.
2.
Sagar KB, Rhyne TL, Warltier DC, Pelc LR, Wann LS.
Intramyocardial variability in integrated backscatter: effects of
coronary occlusion and reperfusion. Circulation. 1987;75:436-442.
3. Wickline SA, Thomas LJ, Miller JG, Sobel BE, Perez JE. A relationship between integrated backscatter and myocardial contractile function. J Clin Invest. 1988;76:2151-2160.
4. Wear KA, Shoup TA, Popp RL. Ultrasonic tissue characterization of canine myocardial contraction. IEEE Trans Ultrasonics Ferroelectrics Frequency Control. 1986;33:347-353. [Medline] [Order article via Infotrieve]
5. O'Donnell M, Mimbs JW, Miller JG. Relationship between collagen and ultrasonic backscatter in myocardial tissue. J Acoust Soc Am. 1981;69:580-588. [Medline] [Order article via Infotrieve]
6. Shung KK, Reid JM. Ultrasonic scattering from tissue. 1977 Ultrasonics Symposium Proceedings, IEEE catalog no. 77CH1264-ISU, 230, 1977.
7. Rhyne TL, Sagar KB, Wann SL, Haasler G. The myocardial signature: absolute backscatter, cyclic variation, frequency variation and statistics. Ultrason Imaging. 1986;8:107-120. [Medline] [Order article via Infotrieve]
8.
Sagar KB, Pelc LR, Rhyne TL, Wann LS, Warltier DC. Influence
of heart rate, preload, afterload, and inotropic state on myocardial
ultrasonic backscatter. Circulation. 1988;77:478-486.
9. Marangore RD, Glasser AA, Mosi JS, Brody AS, Beckwith TH, Walter GR, White WL. Effects of storage and handling techniques on skin tissue properties. Ann N Y Acad Sci. 1966;136:439-454.
10. Gellski JV, Shung KK. Studies on acoustic impedance of major bovine blood vessel walls. J Acoust Soc Am. 1983;71:467-470.
11.
Sagar KB, Agemura DH, O'Brien WD Jr, Pelc LR, Rhyne TL,
Wann
LS, Komorowski RA, Warltier DC. Quantitative ultrasonic assessment of
normal and ischaemic myocardium with an acoustic microscope:
relationship to integrated backscatter. Cardiovasc Res. 1990;24:447-455.
12. Tervola KMU, Foster SC, O'Brien WD Jr. Attenuation coefficient measurement technique at 100 MHz with the scanning laser acoustic microscope. IEEE Trans Sonics Ultrasonics. 1985;SU-32:259-265.
13. Tervola KMU, O'Brien WD Jr. Spatial frequency domain technique: an approach for analyzing the scanning laser acoustic microscope interferogram images. IEEE Trans Sonics Ultrasonics. 1985;SU-32:544-554.
14. Olerud JE, O'Brien WD Jr, Reiderer-Henderson MA, Steiger DL, Forster FK, Daley C, Ketterer DJ, Odland GF. Ultrasonic assessment of skin and wounds with the scanning laser acoustic microscope. J Invest Dermatol. 1987;88:615-623. [Medline] [Order article via Infotrieve]
15. Steiger DL, O'Brien WD Jr, Olerud JE, Reiderer-Henderson MA, Odland GF. Measurement uncertainty assessment of the scanning laser acoustic microscope and application to canine skin and wound. IEEE Trans Ultrasonics Ferroelectrics Frequency Control. 1988;35:741-748. [Medline] [Order article via Infotrieve]
16. Embree PM, Tervola KMU, Foster SG, O'Brien WD Jr. Spatial distribution of the speed of sound in biological materials with the scanning laser acoustic microscope. IEEE Trans Sonics Ultrasonics. 1985;SU-32:341-350.
17. Nicozisin DD. An automated image data acquisition and analysis system for the scanning laser acoustic microscope. Master of Science Thesis, University of Illinois, 1989.
18. Dunn F. Ultrasonic properties of biological media. In: Melner R, Rosenfield E, Cobet U, eds. Ultrasound Interactions in Biology and Medicine. New York, NY: Plenum Publishing Corp; 1983:1-6.
19. O'Brien WD Jr. The role of collagen in determining ultrasonic propagation properties in tissues. In: Kessler LW, ed. Acoustical Holography. New York, NY: I. Plenum Press; 1977:37-50.
20. Wear KA, Milunski MR, Wickline SA, Perez JE, Sobel BE, Miller JG. Contraction related variation in frequency dependence of acoustic properties of canine myocardium. J Acoust Soc Am. 1989;86:2067-2072. [Medline] [Order article via Infotrieve]
21. Mottley JG, Miller JG. Anisotropy of ultrasonic attenuation in soft tissue measurements in vitro. J Acoust Soc Am. 1990;88:1203-1210. [Medline] [Order article via Infotrieve]
This article has been cited by other articles:
 |
|
 |
|
  A. Micari, M. Pascotto, A. R. Jayaweera, J. Sklenar, N. C. Goodman, and S. Kaul Cyclic variation in ultrasonic myocardial integrated backscatter is due to phasic changes in the number of patent myocardial microvessels. J. Ultrasound Med., August 1, 2006; 25(8): 1009 - 1019. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Lasserre, P. Gosse, and S. Mansour Myocardial Tissue Characterization in Echocardiography with Videodensitometry: Evaluation of a New Semi-automatic Software Applied on a Population of Hypertensive Patients Eur J Echocardiogr, December 1, 2003; 4(4): 292 - 299. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Giglio, V. Pasceri, L. Messano, F. Mangiola, L. Pasquini, A. Dello Russo, A. Damiani, M. Mirabella, G. Galluzzi, P. Tonali, et al. Ultrasound tissue characterization detectspreclinical myocardial structural changes inchildren affected by Duchenne muscular dystrophy J. Am. Coll. Cardiol., July 16, 2003; 42(2): 309 - 316. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Koyama, P. A. Ray-Sequin, and R. H. Falk Prognostic Significance of Ultrasound Myocardial Tissue Characterization in Patients With Cardiac Amyloidosis Circulation, July 30, 2002; 106(5): 556 - 561. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. Dagdeviren, O. Akdemir, M. Eren, O. Bolca, E. Oguz, Y. Gurlertop, and T. Tezel Prognostic implication of myocardial texture analysis in idiopathic dilated cardiomyopathy Eur J Heart Fail, January 1, 2002; 4(1): 41 - 48. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Imasaka, S. Morita, I. Nagano, M. Masuda, R. Tominaga, and H. Yasui Coronary artery bypass grafting on the beating heart evaluated with integrated backscatter Ann. Thorac. Surg., September 1, 2000; 70(3): 1049 - 1053. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Masugata, S. Senda, A. Kinoshita, Xin Lu, H. Sakamoto, S. Sakamoto, H. Matsuo, and K. Mizushige Tissue Characterization of Myocardial Cells by Use of High-Frequency Acoustic Microscopy: Differential Myocyte Sound Speed and Its Transmural Variation in Normal, Pressure-Overload Hypertrophic, and Amyloid Myocardium Angiology, October 1, 1999; 50(10): 837 - 845. [Abstract] [PDF]
|
|
|
|
|
|
H. Masugata, K. Mizushige, S. Senda, Xin Lu, A. Kinoshita, H. Sakamoto, S. Nozaki, S. Sakamoto, and H. Matsuo Evaluation of Left Atrial Wall Elasticity Using Acoustic Microscopy Angiology, July 1, 1999; 50(7): 583 - 590. [Abstract] [PDF]
|
|
|
|
 |
|
 V. Di Bello, R. Pedrinelli, D. Giorgi, A. Bertini, L. Talarico, M. T. Caputo, B. Massimiliano, G. Dell'Omo, M. Paterni, and C. Giusti Ultrasonic Videodensitometric Analysis of Two Different Models of Left Ventricular Hypertrophy : Athlete's Heart and Hypertension Hypertension, April 1, 1997; 29(4): 937 - 944. [Abstract] [Full Text]
|
|
|
|
 |
|
 E. K. Louie and D. S. Louie New Echocardiographic Technology: Does it Add to Clinical Decision-Making? Seminars in Cardiothoracic and Vascular Anesthesia, March 1, 1997; 1(1): 16 - 31. [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||